Skip to main content
SpringerLink
Log in

Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate?

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary.

The cytology of leaf cells from five different high-alpine plants was studied and compared with structures in chloroplasts from the typical high-alpine plant Ranunculus glacialis previously described as having frequent envelope plus stroma protrusions. The plants under investigation ranged from subalpine/alpine Geum montanum through alpine Geum reptans, Poa alpina var. vivipara, and Oxyria digyna to nival Cerastium uniflorum and R. glacialis. The general leaf structure (by light microscopy) and leaf mesophyll cell ultrastructure (by transmission electron microscopy [TEM]) did not show any specialized structures unique to these mountain species. However, chloroplast protrusion formation could be found in G. reptans and, to a greater extent, in O. digyna. The other species exhibited only a low percentage of such chloroplast structural changes. Occurrence of protrusions in samples of G. montanum and O. digyna growing in a mild climate at about 50 m above sea level was drastically reduced. Serial TEM sections of O. digyna cells showed that the protrusions can appear as rather broad and long appendices of plastids, often forming pocketlike structures where mitochondria and microbodies are in close vicinity to the plastid and to each other. It is suggested that some high-alpine plants may form such protrusions to facilitate fast exchange of molecules between cytoplasm and plastid as an adaptation to the short, often unfavorable vegetation period in the Alps, while other species may have developed different types of adaptation that are not expressed in ultrastructural changes of the plastids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

TEM:

transmission electron microscopy

References

  • Bergweiler P (1987) Charakterisierung von Bau und Funktion der Photosynthesemembran ausgewählter Pflanzen unter den Extrembedingungen des Hochgebirges. PhD thesis, University of Cologne, Cologne, Federal Republic of Germany

  • WD Billings PJ Godfrey BF Chabot DP Bourque (1971) ArticleTitleMetabolic acclimation of temperature in arctic and alpine ecotypes of Oxyria digyna Arct Alp Res 3 277–289 Occurrence Handle10.2307/1550044

    Article  Google Scholar 

  • M Blumthaler AR Webb G Seckmeyer AF Bais M Huber B Mayer (1994) ArticleTitleSimultaneous spectroradiometry: a study of solar UV irradiance at two altitudes Geophys Res Lett 21 2805–2808 Occurrence Handle10.1029/94GL02786

    Article  Google Scholar 

  • TM Bourett KJ Czymmek RJ Howard (1999) ArticleTitleUltrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing Planta 208 472–479 Occurrence Handle10.1007/s004250050584 Occurrence Handle1:CAS:528:DyaK1MXktlSrtr0%3D

    Article  CAS  Google Scholar 

  • O Buchner C Lütz A Holzinger (2007) ArticleTitleDesign and construction of a new temperature controlled chamber for light- and confocal microscopy under monitored conditions: biological applications for plant samples J Microsc 225 183–191 Occurrence Handle17359253 Occurrence Handle10.1111/j.1365-2818.2007.01730.x Occurrence Handle1:CAS:528:DC%2BD2sXmt1Gnsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • G De Santis-Maciossek W Kofer A Bock S Schoch RM Maier G Wanner W Rüdiger H-U Koop RG Herrmann (1999) ArticleTitleTargeted disruption of the plastid RNA polymerase genes rpoA, B and C1: molecular biology, biochemistry and ultrastructure Plant J 18 477–489 Occurrence Handle10417698 Occurrence Handle10.1046/j.1365-313X.1999.00473.x Occurrence Handle1:CAS:528:DyaK1MXkvFektb4%3D

    Article  PubMed  CAS  Google Scholar 

  • L Engel H Fock C Schnarrenberger (1986a) ArticleTitleCO2 and H2O gas exchange of the high alpine plant Oxyria digyna (L.) HILL 1. Irradiance and temperature dependence Photosynthetica 20 293–303

    Google Scholar 

  • L Engel H Fock C Schnarrenberger (1986b) ArticleTitleCO2 and H2O gas exchange of the high alpine plant Oxyria digyna (L.) HILL 2. Response to high irradiance stress and supraoptimal leaf temperatures Photosynthetica 20 304–314

    Google Scholar 

  • N Engel M Schmidt C Lütz J Feierabend (2006) ArticleTitleMolecular identification, heterologous expression and properties of light-intensive plant catalases Plant Cell Environ 29 593–607 Occurrence Handle17080610 Occurrence Handle10.1111/j.1365-3040.2005.01439.x Occurrence Handle1:CAS:528:DC%2BD28Xksl2nu7g%3D

    Article  PubMed  CAS  Google Scholar 

  • K Esau (1969) Pflanzenanatomie Gustav Fischer Stuttgart

    Google Scholar 

  • TP Freeman ME Duysen (1975) ArticleTitleThe effect of imposed water stress on the development and ultrastructure of wheat chloroplasts Protoplasma 83 131–145 Occurrence Handle10.1007/BF01289336

    Article  Google Scholar 

  • I Gielwanowska E Szczuka (2005) ArticleTitleNew ultrastructural features of organelles in leaf cells of Deschampsia antarctica Desv Polar Biol 28 951–955 Occurrence Handle10.1007/s00300-005-0024-2

    Article  Google Scholar 

  • JC Gray JA Sullivan JM Hibberd MR Hansen (2001) ArticleTitleStromules: mobile protrusions and interconnections between plastids Plant Biol 3 223–233 Occurrence Handle10.1055/s-2001-15204 Occurrence Handle1:CAS:528:DC%2BD3MXlvFGhsLc%3D

    Article  CAS  Google Scholar 

  • BES Gunning (2005) ArticleTitlePlastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, branching, bridging, and tip-shedding Protoplasma 225 33–42 Occurrence Handle15868211 Occurrence Handle10.1007/s00709-004-0073-3

    Article  PubMed  Google Scholar 

  • U Heber R Bligny P Streb R Douce (1996) ArticleTitlePhotorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinhibition under sunlight Bot Acta 109 307–315 Occurrence Handle1:CAS:528:DyaK28XlsVGqu7g%3D

    CAS  Google Scholar 

  • OM Heide (2005) ArticleTitleEcotypic variation among European arctic and alpine populations of Oxyria digyna Arct Antarct Alp Res 37 233–238 Occurrence Handle10.1657/1523-0430(2005)037[0233:EVAEAA]2.0.CO;2

    Article  Google Scholar 

  • A Holzinger G Wasteneys C Lütz (2007a) ArticleTitleInvestigating cytoskeletal function in chloroplast protrusion formation in the arctic-alpine plant Oxyria digyna Plant Biol 9 400–410 Occurrence Handle10.1055/s-2006-924727 Occurrence Handle1:STN:280:DC%2BD2szktFGiug%3D%3D

    Article  CAS  Google Scholar 

  • A Holzinger O Buchner C Lütz MR Hanson (2007b) ArticleTitleTemperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana Protoplasma 230 23–30 Occurrence Handle10.1007/s00709-006-0222-y Occurrence Handle1:STN:280:DC%2BD2s7ltFWnug%3D%3D

    Article  CAS  Google Scholar 

  • RH Köhler MR Hanson (2000) ArticleTitlePlastid tubules of higher plants are tissue-specific and developmentally regulated J Cell Sci 113 81–89 Occurrence Handle10591627

    PubMed  Google Scholar 

  • C Körner (2003) Alpine plant life EditionNumber2 Springer Berlin Heidelberg New York

    Google Scholar 

  • W Larcher (2001) Ökophysiologie der Pflanzen EditionNumber6 Ulmer Stuttgart

    Google Scholar 

  • W Larcher J Wagner (1976) ArticleTitleTemperaturgrenzen der CO2-Aufnahme und Temperaturresistenz der Blätter von Gebirgspflanzen im vegetationsaktiven Zustand Oecol Plant 11 361–374

    Google Scholar 

  • W Larcher J Wagner C Lütz (1997) ArticleTitleThe effect of heat on photosynthesis, dark respiration and cellular ultrastructure of the arcticalpine psychrophyte Ranunculus glacialis Photosynthetica 34 219–232 Occurrence Handle10.1023/A:1006840623763 Occurrence Handle1:CAS:528:DyaK1cXmtFKgtw%3D%3D

    Article  CAS  Google Scholar 

  • G Lehner C Lütz (2003) ArticleTitlePhotosynthetic functions of cembran pines and dwarf pines during winter at timberline as regulated by different temperatures, snowcover and light J Plant Physiol 160 153–166 Occurrence Handle12685031 Occurrence Handle10.1078/0176-1617-00798 Occurrence Handle1:CAS:528:DC%2BD3sXivVWgsb4%3D

    Article  PubMed  CAS  Google Scholar 

  • M Lundmark A Cavaco S Trevanion V Hurry (2006) ArticleTitleCarbon partitioning and export in transgenic Arabidopsis thaliana with altered capacity for sucrose synthesis grown at low temperature: a role for metabolite transporters Plant Cell Environ 29 1703–1714 Occurrence Handle16913860 Occurrence Handle10.1111/j.1365-3040.2006.01543.x Occurrence Handle1:CAS:528:DC%2BD28XhtVWktLjM

    Article  PubMed  CAS  Google Scholar 

  • C Lütz (1981) ArticleTitleDevelopment and ageing of etioplast structures in dark grown leaves of Avena sativa L Protoplasma 108 83–98 Occurrence Handle10.1007/BF01276885

    Article  Google Scholar 

  • C Lütz (1987) ArticleTitleCytology of high alpine plants II. Microbody activity in leaves of Ranunculus glacialis L Cytologia 52 679–686

    Google Scholar 

  • C Lütz (1996) ArticleTitleAvoidance of photoinhibition and examples of photodestruction in high alpine Eriophorum J Plant Physiol 148 120–128

    Google Scholar 

  • C Lütz P-G Gülz (1985) ArticleTitleComparative analysis of epicuticular waxes from some high alpine plant species Z Naturforsch C 40 599–605

    Google Scholar 

  • C Lütz W Moser (1977) ArticleTitleBeiträge zur Cytologie hochalpiner Pflanzen. I. Untersuchungen zur Ultrastruktur von Ranunculus glacialis L Flora 166 21–34

    Google Scholar 

  • C Lütz E Schönauer G Neuner (2005) ArticleTitlePhysiological adaptation before and after snow melt in green overwintering leaves of some alpine plants Phyton 45 139–156

    Google Scholar 

  • N Manuel G Cornic S Aubert P Choler R Bligny U Heber (1999) ArticleTitleProtection against photoinhibition in the alpine plant Geum montanum Oecologia 119 149–158 Occurrence Handle10.1007/s004420050771

    Article  Google Scholar 

  • HA Mooney WD Billings (1961) ArticleTitleComparative physiological ecology of arctic and alpine populations of Oxyria digyna Ecol Monogr 31 1–29 Occurrence Handle10.2307/1950744

    Article  Google Scholar 

  • W Moser (1970) ArticleTitleÖkophysiologische Untersuchungen an Nivalpflanzen Mitt Ostalp-din Ges Vegetkd 11 121–134

    Google Scholar 

  • W Moser W Brzoska K Zachhuber W Larcher (1977) ArticleTitleErgebnisse des IBP-Projekts “Hoher Nebelkogel 3184 m” Sitzungsber Österr Akad Wiss Math-Naturwiss Kl Abt 1 186 387–419

    Google Scholar 

  • SKA Natesan JA Sullivan JC Gray (2005) ArticleTitleStromules: a characteristic cell-specific feature of plastid morphology J Exp Bot 56 787–797 Occurrence Handle15699062 Occurrence Handle10.1093/jxb/eri088 Occurrence Handle1:CAS:528:DC%2BD2MXit1Knuro%3D

    Article  PubMed  CAS  Google Scholar 

  • EH Newcomb (1967) ArticleTitleFine structure of protein-storing plastids in bean root tips J Cell Biol 33 143–163 Occurrence Handle6033932 Occurrence Handle10.1083/jcb.33.1.143 Occurrence Handle1:STN:280:CCiB3cbltFw%3D

    Article  PubMed  CAS  Google Scholar 

  • P Nick (2000) Plant microtubules: potential for biotechnology Springer Berlin Heidelberg New York

    Google Scholar 

  • ES Reynolds (1963) ArticleTitleThe use of lead citrate at high pH as an electronopaque stain in electron microscopy J Cell Biol 17 208–212 Occurrence Handle13986422 Occurrence Handle10.1083/jcb.17.1.208 Occurrence Handle1:CAS:528:DyaF3sXktVClu70%3D

    Article  PubMed  CAS  Google Scholar 

  • H-A Schäfers J Feierabend (1976) ArticleTitleUltrastructural differentiation of plastids and other organelles in rye leaves with a high-temperature-induced deficiency of plastid ribosomes Cytobiologie 14 75–90

    Google Scholar 

  • K Schwarzerová J Petrášek KCS Panigrahi S Zelenková Z Opatrný P Nick (2006) ArticleTitleIntranuclear accumulation of plant tubulin in response to low temperature Protoplasma 227 185–196 Occurrence Handle16736258 Occurrence Handle10.1007/s00709-005-0139-x

    Article  PubMed  Google Scholar 

  • AR Spurr (1969) ArticleTitleA low-viscosity epoxy resin embedding medium for electron microscopy J Ultrastruct Res 26 31–43 Occurrence Handle4887011 Occurrence Handle10.1016/S0022-5320(69)90033-1 Occurrence Handle1:CAS:528:DyaF1MXkvVahsLc%3D

    Article  PubMed  CAS  Google Scholar 

  • P Streb J Feierabend R Bligny (1997) ArticleTitleResistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants Plant Cell Environ 20 1–11 Occurrence Handle10.1111/j.1365-3040.1997.tb00679.x

    Article  Google Scholar 

  • P Streb S Aubert E Gout R Bligny (2003) ArticleTitleReversibility of cold- and light-stress tolerance and accompanying changes of metabolite and antioxidant levels in the two high mountain plant species Soldanella alpina and Ranunculus glacialis J Exp Bot 54 405–418 Occurrence Handle12493869 Occurrence Handle10.1093/jxb/54.381.405 Occurrence Handle1:CAS:528:DC%2BD3sXhtlOhsrs%3D

    Article  PubMed  CAS  Google Scholar 

  • P Streb E-M Josse E Gallouët F Baptist M Kuntz G Cornic (2005) ArticleTitleEvidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain species Ranunculus glacialis Plant Cell Environ 28 1123–1135 Occurrence Handle10.1111/j.1365-3040.2005.01350.x Occurrence Handle1:CAS:528:DC%2BD2MXhtVGltrfN

    Article  CAS  Google Scholar 

  • D Taschler G Neuner (2004) ArticleTitleSummer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary Plant Cell Environ 27 737–746 Occurrence Handle10.1111/j.1365-3040.2004.01176.x

    Article  Google Scholar 

  • B Wildi C Lütz (1996) ArticleTitleAntioxidant composition of selected high alpine plant species from different altitudes Plant Cell Environ 19 138–146 Occurrence Handle10.1111/j.1365-3040.1996.tb00235.x Occurrence Handle1:CAS:528:DyaK28XitVyjt78%3D

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Botany, University of Innsbruck, Innsbruck

    C. Lütz

  2. U.S. Army Center for Health Promotion and Preventive Medicine – Europe, Landstuhl

    L. Engel

Authors
  1. C. Lütz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Lütz.

Additional information

Correspondence and reprints: Institute of Botany, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lütz, C., Engel, L. Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate?. Protoplasma 231, 183–192 (2007). https://doi.org/10.1007/s00709-007-0249-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-007-0249-8

Search

Navigation